The 21st century is a noisy place: sirens, alarms, cars, mobile phones; you have to go a long way get any peace. But for the first 100 million years after the earliest terrestrial ancestors heaved themselves on to land, they may have heard little of the surrounding soundscape. ‘It is quite a different task to detect sound in water and air as the physical properties of these two media are very different’, says Christian Christensen from Aarhus University, Denmark. Sound vibrations that are transmitted through water pass with ease into the bodies of aquatic animals, to vibrate minute granules (otoliths) in the animals' ears to produce the sensation of hearing. However, as soon as the first tetrapods emerged from the water, the water-borne mechanism of sound transmission may have failed as the vast majority of vibrations that are carried in air are reflected when they reach a body. How the modern tetrapod ear – which transforms aerial sound pressure waves into physical vibrations in the inner ear – evolved from these humble beginnings is something of a mystery. However, modern lung fish may hold the key to this puzzle. ‘Lungfish are the closest living relatives of tetrapods’, explains Christensen, who wondered whether they may hear sound using mechanisms that are similar to those of our ancient ancestors. So, Christensen and his colleagues, Jakob Christensen-Dalsgaard and Peter Madsen, began investigating the terrestrial hearing of these remarkable air-breathing fish (p. 381).

The researchers explain that the fish could use their air-filled lungs to convert pressure waves into vibrations – in much the same way as the ear drum (tympanum) converts sound pressure into physical vibrations – and so they designed a 2 m long steel tube that they filled with water to test the fish's hearing. By placing a loud speaker at one end of the tube and playing a pure note of one frequency in the water, they could generate a standing wave where the pressure was high at locations where the water particles were stationary and the pressure was low when the particles were moving most. Positioning an anaesthetised lungfish at various positions along the length of the tube – to vary the sound pressure acting on them – and measuring the fish's hearing by recording electrical activity in the brainstem, Christensen found that the fish were able to hear sound pressure at frequencies above 200 Hz, while hearing particle motion at lower frequencies.

African lungfish (Protopterus annectens). Photo credit: Cedricguppy – Loury Cédric [CC BY-SA 4.0], via Wikimedia Commons.

African lungfish (Protopterus annectens). Photo credit: Cedricguppy – Loury Cédric [CC BY-SA 4.0], via Wikimedia Commons.

Next, he measured the volume of the air in the fish's lungs using computed tomography and found that the lung's resonant frequency was 320 Hz, which means that the lungs are perfectly attuned to generate the strongest vibrations at frequencies where the lungfish hear the sound pressure. ‘This strongly suggests that pressure detection in lungfish is enabled through detection of the pressure-induced particle motion generated by the resonating air volumes in the lungs’, says Christensen.

But would this mean that the fish could hear in air too? Christensen recorded the brainstem activity of the fish in response to airborne sounds ranging in frequency from 80 to 1280 Hz and the team were impressed to see that the fish could hear loud sounds (above 85 dB SPL) at frequencies up to 200 Hz. ‘It was a surprise that the lungfish, being completely unadapted to hearing, were in fact able to hear airborne sound’, says Christensen, who suspects that our earliest terrestrial may not have been as deaf as we thought. ‘Even aquatic vertebrates with no middle ear adaptations to aerial hearing, such as the early atympanic tetrapod Acanthostega, may have been able to detect higher levels of low frequency airborne sound’, he says.

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Hearing of the African lungfish (Protopterus annectens) suggests underwater pressure detection and rudimentary aerial hearing in early tetrapods
J. Exp. Biol.